CHAPTER 1 Introduction On such a silent night a silvery jet was seen far in advance of the white bubbles at the bow. Lit up by the moon, it looked celestial; seemed some plumed and glittering god uprising from the sea. –Moby Dick 1.1 Introduction Wildlife conservation research is currently dominated by studies into population size and growth, genetics, seasonal movements and reproductive rates. Hormones are key factors in reproductive rates and general health and so are crucial to a population’s survival. Hormones control many basic functions of the body including reproductive systems in addition to the physiological responses to changing environmental parameters. It has been reported that measured hormonal concentrations can offer a better understanding of factors that impair a species’ demographic vitality or identify early warning signals for changes in reproductive rates (Kirby and Ridgway 1984; Schoech and Lipar 1998). In order to successfully manage any population and understand the factors that may be influencing it, basic biological knowledge is required on internal physiology, reproductive cycling, and effects of extraneous factors (such as increasing levels of stress) on both individual animals and populations. The use of non-invasive techniques to monitor hormone metabolites in wildlife is growing (Creel et al. 1991; Lasley and Kirkpatrick 1991; Wasser 1995; Robbins and Czekala 1997; Rolland et al. 2005). These techniques can be used to determine reproductive fitness and further our understanding of the relationship between behaviour, physiology and the environment (Wildt and Wemmer 1999). 1 Chapter 1 – Introduction With advances in technology, animal reproductive parameters in wildlife populations, such as hormone concentrations and reproductive cycling, have been described for a number of terrestrial mammal species including: bandicoots (Gemmell et al. 1985); Asian elephants (Brown et al. 1991); black rhinoceroses (Berkeley et al. 1997); gorillas (Czekala and Robbins 2001); feral horses (Lasley and Kirkpatrick 1991); Siberian tigers (Seal et al. 1985); one-humped camels (Marie and Anouassi 1987); and muriquis (Ziegler et al. 1997). Although not as prominent as their terrestrial counterparts, there has been some description of reproductive cycling in marine mammal species such as killer whales (Duffield et al. 1995); polar bears (Ramsay and Stirling 1988); harbour seals (Raeside and Ronald 1981); and captive bottlenose and common dolphins (Kirby and Ridgway 1984). There are a number of advantages in studying terrestrial mammals over marine mammals as they are easier to locate, can be anaesthetised, tracked, and tagged with relative ease. In contrast, marine mammals provide researchers with a number of complex problems when assessing their basic biology and internal physiology. When comparing marine mammals, pinnipeds (seals and sea lions) and polar bears and sea otters can be accessed when they come ashore to breed or rest, but cetaceans (whales and dolphins) and sirenians (dugongs and manatees) do not come ashore at all and novel methods must be developed. Hormone concentrations are determined after collection of a sample through invasive techniques such as blood (plasma or serum) sampling or through non-invasive techniques, such as faecal or urine sampling. Obtaining samples for hormone analysis from cetaceans can be difficult because of their aquatic locations. Anaesthesia of cetaceans, although possible, has only been accomplished by a few individuals (Haulena and Heath 2001) and therefore is not common practice, 2 Chapter 1 – Introduction particularly with wild animals. Blood sampling has been achieved in captive cetaceans (Duffield et al. 1995; Suzuki et al. 1998) and in some smaller wild cetaceans (St. Aubin et al. 1996) but unfortunately with fatal results in great whales (Kjeld et al. 1992; Kjeld 2001; Suzuki et al. 2001; Kjeld et al. 2004). Mansour et al. (2002) recently developed a protocol to assess progesterone concentrations in the blubber of minke whales using whales from the Greenland hunt. They suggest that blubber from biopsy sampling may be another way to assess hormone concentrations in great whales. Captive cetaceans have been trained for urine sampling (Robeck et al. 1993; 1994; Duffield et al. 1995) although some species can be particularly difficult to train (G. Bedford, personal communication). Faecal sampling has been undertaken in the North Atlantic right whale (Rolland et al. 2005) but can be difficult as great whales do not defecate at regular intervals and tend to defecate only when in their feeding grounds. Faecal sampling has been also used to determine stress in some seal species (Gulland et al. 1999; Hunt et al. 2004; Mashburn and Atkinson 2004). Most great whales migrate annually from their breeding grounds, usually in warmer tropical waters at low latitudes, to their feeding grounds in cooler Artic or Antarctic waters at high latitudes (Dawbin 1966). As there is little to no feeding on the breeding grounds or along the migratory route, faecal samples can only be systematically collected in the feeding grounds. In the Northern Hemisphere, this is in the Arctic or Sub-Arctic areas which are readily accessible and for the coastal great whales, such as humpback whales and right whales, close to shore. In the Southern Hemisphere, faecal sampling is more difficult as the feeding areas are in the Southern Ocean near Antarctica and systematic samples cannot be easily obtained. 3 Chapter 1 – Introduction Assessment of the internal physiology (such as reproductive hormone concentrations) of great whales and other large cetaceans is problematic without restraint, which can endanger the animal and the lives of those that attempt it. Currently the only reproductive hormone data of great whales comes from commercial whaling on minke whales and fin whales (Kjeld 2001; Suzuki et al. 2001; Mansour et al. 2002). Subsistence whaling in the Arctic on bowhead whales also allows for further opportunity to assess hormone concentrations in some great whale species (Reeves et al. 2001). The challenge remains to assess hormone concentrations of large free-swimming whales without harm and to sample the population multiple times over a given period to gain a better understanding of their basic biology. Reproduction and population growth are fundamental to whale conservation. In this chapter I will present our current understanding of mammalian reproductive hormones; review our current knowledge of cetacean reproductive hormones; discuss the suitability of using existing non-invasive techniques to determine reproductive hormones in cetaceans; and propose a new non-invasive method to determine reproductive hormones in free-swimming whales. 4 Chapter 1 – Introduction 1.2. Whales and whaling There are two suborders in the order Cetacea, the Odontoceti (toothed whales) and the Mysticeti (baleen whales). The great whales are all those species found in the Mystecti, including humpback, right and fin whales; and one species of Odontoceti, sperm whales. Great whale populations have been hunted from the time of the early Basque whalers in the sixteenth century to the present day. Commercial whaling catch limits were set to zero by the International Whaling Commission in 1982, coming into effect in 1986 (IWC Convention III-11). Scientific and subsistence whaling continues today. With the decline of whales in the Atlantic in the 1800s, many European and American whaling ships moved to the Indian, Pacific and Southern Oceans. Until the late 1890s whales were hunted from shore-based stations and so whalers were limited in their catches by the number they could tow back to shore. The factory ship and the exploding harpoon were invented in the early 1900s (Harmer 1931; Day 1992). This meant that more whales could be caught and processed at sea, producing a sharp decline in great whale stocks in Antarctic waters. Humpback whales in Antarctic waters were divided into six areas designated by their respective feeding areas (fig. 1.1). The areas were originally designated according to whaling areas in the Antarctic and are now used to describe the different feeding and breeding populations. Dawbin (1966) describes how those animals found in particular feeding areas in the Southern Ocean tend to be found in specific breeding areas as well. The whales off the west coast of Australia are known as the Area IV (70 oE- 130 oE) population and, off the east coast as the Area V (130 oE-170 oW) population (Dawbin 1966). Area V humpback whales are thought to migrate up the east coast of 5 Chapter 1 – Introduction Figure 1.1: World map depicting the six areas of the Antarctic as designated by the International Whaling Commission (IWC). 6 7 7 Equator Area VI Area I Area II Area III Area IV Area V 120 oW 60 oW 0o 70 oE 130 oE 170 oW Chapter 1 – Introduction Australia as well as New Zealand and Tonga. Prior to whaling in Australian waters it was estimated that there were approximately 17,000 humpback whales in Area IV (Bannister 1994) and 10,000 humpback whales off the east coast, a portion of the Area V population (Paterson and Paterson 1984). The portion of the Area V humpback whale stock that migrates along the east Australian coast is estimated to have numbered 1900 ± 250 in 1992 compared with as few as 100 at the conclusion of commercial whaling in 1962. The average annual rate of increase from 1984 to 1992 was estimated at 11.7% with a 95% confidence interval of 9.6-13.8% (Paterson et al. 1994). Brown et al. (2003) estimated the annual rate of increase to be 8.54% (s.e. = 0.05) from 1991 to 2000. This level of recovery is at a higher limit for a large mammal. This suggests that there have been no detrimental environmental impacts upon this particular stock post whaling (Paterson et al. 1994). In 1946, the International Whaling Commission (IWC) was established to monitor catch rates and quotas for the whaling industry. As the number of whales decreased the IWC became responsible for the protection of the great whales.